Evaluation of Periodontal Tissues in Growing Patients with Bilateral Cleft Lip and Palate. a Pilot Study

Abstract Aim To evaluate the periodontal status, mucogingival parameters and oral hygiene in growing patients with bilateral cleft lip and palate. Material and methods Assessment was performed in 15 patients aged 6 to 18 years with a bilateral cleft. Records included probing pocket depth, clinical attachment level, keratinized gingiva, recession, vestibule depth, biotype, type of fraena, dental plaque and bleeding. Results The mean scores of pocket depth were: 1.9 mm for central incisors, 1.6 mm for lateral incisors, 1.7 mm for canines, 2.0 mm for first premolars. There were only a few teeth with minimal attachment loss (1 mm). Gingival recessions were not recorded. High scores were recorded for the hygiene indicator, especially on the buccal, mesial and distal surfaces. Due to soft and hard tissue malformations, it was difficult to precisely assess the biotype and keratinized gingiva. However, keratinized gingiva was narrower near the teeth adjacent to the cleft. Similarly, the vestibule was shallower in this area. In 12 out of 15 children it was impossible to define the type of labial fraenum. Conclusions Evaluation of the periodontal status is important for successful comprehensive rehabilitation in cleft patients. Specific features of hard (alveolar process) and soft tissue (scars, unusual fraena) malformations caused by the cleft and previous surgical procedures have functional and morphological implications. Narrower gingiva and a shallower vestibule in the presence of dental plaque and bleeding are unfavourable conditions to maintain a healthy periodontium. It is essential to include periodontal assessment and preventive treatment to a comprehensive approach as early as possible.


INTRODUCTION
Cle lip, alveolus, and palate are congenital malformations created in the early phase of embryogenesis [1]. e aetiology is unknown, but it is considered to be complex. Some cle lips and palates have a genetic origin, others may be caused by environmental factors [2]. Children with a cle require multidisciplinary treatment due to problems during feeding, speaking, listening, as well as frequent ear infections and psychosocial issues [2,3].
Although surgery is performed in the rst few months of life, most children have a de ciency of so tissues, bone volume, malformation and/or lack of teeth at the cle site [4]. ese features, as well as side e ects of surgeries itself (scars, unusual fraena attachments), cause obstacles during orthodontic and restorative treatment and negatively in uence aesthetics. Children with cle s need orthodontic treatment, which provides alignment and stabilization of the teeth a er reconstructive procedures [5]. e timing of bone gra placement is an important issue. e most commonly accepted procedure is secondary bone gra ing (during the mixed dentition period) to provide alveolar bone support for the erupting teeth. Bone gra ing in adults is associated with a higher risk of gra failure due to changes in the healing potential caused by the age of the patient [5,6]. According to some studies, early performance of secondary gingivoalveoloplasty combined with hard palate closure at the age of 18-36 months makes it possible to avoid bone gra ing in the future. Permanent tooth eruption occurs at a normal rate, without the need for secondary alveolar bone gra ing [7]. e one-stage surgery method seems to improve anatomical conditions in the craniofacial area and enables better further development [8]. Bone gra ing performed a er eruption of the canine may lead to insu cient marginal bone height and gingival recession at the teeth adjacent to the cle . In addition, the vestibular ap technique used to cover the bone gra s, may result in so tissue scars and shallow vestibule, which demand additional surgical procedures [5,6,9].
Moreover, it is important to emphasize that the boundary structures of the oral vestibule have not been formed properly and should be reconstructed as well. On the other hand the vestibular ap technique performed to cover bone gra s in early childhood may result in a scarred and shallower vestibule with loose folds of mucosa [9].
is problem may have functional, hygienic and aesthetic implications. e normal function and appearance of the lip is only possible when the lip can freely move over the teeth during speaking and smiling. e depth of the vestibule is important to protect against infection and functional muscle forces created during eating. In case of an inadequately formed vestibule, additional stress is placed on the attached gingiva in patients with bilateral cle . is could potentially cause mucogingival (gingival recessions) and periodontal problems (periodontal disease). Moreover, a malformed vestibule may have a negative in uence on dentition status and on the maintenance of oral hygiene. e normal depth of the oral vestibule enables prosthodontic and orthodontic treatment [7,9,10].
Furthermore, it is a well-known fact that the smile is characterized by the relationship between the teeth, lips, and gingival tissue. Dental evaluation includes external features, such as: face pro le, smile and lip line, teeth and gingiva exposure during smiling and intra-oral conditions, such as the number of teeth, gingival architecture, biotype, tooth status [11,12]. Planning oral rehabilitation with dentures or implants (usually including orthodontic treatment) depends on the extent of exposure of the gingiva, especially during speaking and smiling. at is why the healthy appearance of the gingiva is important in smile aesthetics [12]. e above reasons justify why periodontal evaluation is directly related to the aesthetic and functional rehabilitation Evaluation of periodontal tissues in growing patients with bilateral cle lip and palate. A pilot study of patients with cle s. Evaluation of periodontal conditions is o en neglected or insu ciently documented, since the patients' major problems are related to reconstructive treatment and quality of life [11,12]. As a result, there are very few studies regarding the periodontal status in cle patients. e aim of the study was to evaluate the periodontal status, mucogingival parameters and hygiene indices in growing patients with bilateral cle lip and palate and to compare the results with other studies.
MATERIAL e sample consisted of consecutively selected patients with complete bilateral cle lip and palate, who were treated in the Orthodontic Department of the Institute of Mother and Child in Warsaw, Poland. 15 Caucasian individuals, aged from 6 to 18 years (nine females and six males) with mixed or permanent dentition were examined. e measurements were performed on eight anterior teeth in the maxilla (102 teeth in total). In seven patients both maxillary lateral incisors were missing, in other four patients one lateral incisor was missing. All the patients underwent reconstructive surgery of the cle lip, alveolar process, hard palate and so palate. Due to maxillary hypoplasia, all the patients were treated with removable or permanent orthodontic appliances. e aim of orthodontic treatment was to achieve a favourable condition for three-dimensional development of the maxilla and to create space for the eruption of permanent teeth. Records were taken between July and November 2015. Exclusion criteria were as follows: the presence of systemic syndromes, hemi-or paraplegia of the face, conditions or/and medication that could in uence bone or so tissue metabolism. A er the examination of the patients, instructions concerning oral hygiene were given depending on individual needs.

METHODS
Clinical examination of the patients was performed using a periodontal probe (Hu-Friedy, PCP UNC 15, calibrated to 1 millimetre). Periodontal examination included records for: Probing pocket depth (PD) measured as the distance from the gingival margin to the bottom of the gingival sulcus. Assessment was carried out at six sites: distolabial, labial, mesiolabial, mesipalatal, palatal and distopalatal.
Clinical attachment level (CAL) measured as the distance from the cementoenamel junction (CEJ) to the bottom of the sulcus. Assessment was carried out at the same six sites as PD.
Gingival Recession (GR) calculated as a distance from CEJ to the gingival margin in case of root exposure. If CEJ was covered by gingiva it meant that there was no recession.
Keratinized gingiva (KG) measured at the labial (midfacial) surface of the tooth as the distance from the gingival margin to the mucogingival junction.
Vestibulum oris depth (VOD) measured as the distance from marginal gingiva to the highest point of the vestibule in relaxed muscle position. e measurements were taken at labial midfacial surfaces of each tooth. e presence of dental plaque was assessed by Plaque Control Record (PCR) according to the O'Leary Plaque Index [13] at four aspects of the tooth: labial, palatal, mesial and distal. A record was considered positive if there was dental plaque on the probing surface. e index was calculated as a percentage, by dividing the number of surfaces containing plaque by the total number of available surfaces and multiplied by 100. e mean PCR scores for every tooth surface and group of teeth were calculated.
Bleeding on probing (BoP) was evaluated according to Ainomo and Bay [14] at six aspects of the tooth: centrolabial, centropalatal, mesiopalatal, distopalatal, mesiolabial, distolabial. A periodontal probe was inserted at the bottom of the sulcus and was moved along the tooth surfaces. If bleeding was noticed, then the examined site was considered positive. e BoP index was calculated in the same way as PCR and mean scores were given as a percentage. e gingival biotype was assessed separately for the maxilla and mandible. e so tissue biotype was classi ed as thin or thick. in biotype was recorded when thin and fragile gingival tissue and a narrow band (width) of keratinized gingiva were detected. ick biotype was recorded when thick, dense and brotic so tissue and a wide band of keratinized gingiva were detected. e type of fraena of the upper and lower lips according to the Placek classi cation [15] was recorded (mucosal, gingival, papillary and penetrating papilla). e presence of additional ligaments and folds, which were results of cle s and reconstructive surgeries, were also recorded.

RESULTS
102 teeth in ten patients were assessed. e data regarding PD, CAL, GR, KG, VOD, PCR, BoP, biotype and labial fraena are summarized in tables. Mean scores for PD for a particular group of teeth were: 1.9 mm for central incisors, 1.6 mm for lateral incisors, 1.7 mm for canines, 2.0 mm for rst premolars (tab. I). ere was only minimal CAL loss, which did not exceed 1 mm (tab. II). Gingival recessions were not observed. High scores for dental plaque (PCR) were recorded on the labial and interproximal (mesial and distal) surfaces contrary to palatal tooth surfaces ( g 2). e mean scores for particular groups of teeth were: 49.5% for central incisors, 38.5% for lateral incisors, 43.5% for canines and 37% for rst premolars (tab. III). e scores for bleeding (BoP) were as follows: 32% for central incisors, 24% for lateral incisors, 27% for canines and 19% for rst premolars (tab. II). KG was narrower near the teeth adjacent to the cle sites. Mean KG at the lateral incisors was 1.3 mm, at the canines 1.9 mm, while at the central incisors KG it was 5.3 mm and 2.7 mm at the rst premolars (tab. IV). e mean VOD was also lower in the cle area. For lateral incisors it was 3.4 mm and 3.8 mm for canines. VODs for premolars and central incisors were higher (5.4 mm and 7.9 mm respectively) (tab. IV).    In 12 out of 15 patients it was impossible to de ne the type of labial fraenum in the maxilla. Two patients had a mucosal type of fraenum attachment and two patients had mucosal types. Due to so tissue malformations (scars, unusual fraena attachments, mucosa folds, additional ligaments), it was di cult to assess the type of gingival biotype in the maxilla ( g. 1, 2). In the mandible nine patients presented thin biotype and six presented a thin biotype.

DISCUSSION
ere are only a few studies on periodontal conditions in growing patients with cle s, In fact the periodontal status may have important implications in the comprehensive treatment of these individuals [16,17,18,19]. Alveolar process de ciency has a negative impact on so tissue appearance, causing functional and aesthetic problems in this area. Additionally, combined de ciencies of hard and so tissues are particularly di cult to treat [4,6,7,8]. Most authors are consistent that patients with cle s are at an increased risk for the development of periodontal disease and carious lesions. However, the data are still limited. Other authors claim that there are no major di erences between the teeth in the cle and the noncle sites regarding periodontal status [20]. Patients with cle s are at high risk of progress of periodontal disease if no supportive periodontal therapy is provided in their early childhood. It has already been presented that adult patients with cle s, high plaque score and gingival in ammation had more periodontal tissue destruction. Moreover, the risk of periodontal disease and the level of tissue disorders increased with age [21]. e aim of this study was to assess the periodontal status in the area of bilateral cle in growing patients.
According to Perdikogianni and co-workers [22], teeth in the cle area had higher pocket probing depths compared with the corresponding teeth in the control group, although pocket depths were up to 3mm, which according to the authors was considered within normal limits. Quirynen and co-workers [20] found only an insigni cant increase in the probing depth of the teeth in the cle site, when compared to the non-cle site. In the study presented there were no gingival pockets deeper than 4 mm. Pockets deeper than normal (>2 mm) but without CAL loss may indicate gingival in ammation or hyperplasia, which results in coronal displacement of the gingival margin. It may be due to the presence of an orthodontic appliance or inadequate plaque control. Established poor oral hygiene may lead to periodontal in ammation with bone loss, because of more pathogenic bacteria subgingivally [23]. e presence of deeper pockets without gingiva in ammation could lead to incomplete tooth eruption, which was also found in some of the patients evaluated.
e few studies that analysed the periodontal status of cle patients showed a high incidence of plaque and bleeding on probing and a high level of periodontal attachment loss [21,24]. In our study there was only minimal CAL loss, which did not exceed 1 mm. Since periodontal parameters worsen with age, this di erence could be due to the young age of the patients in the group evaluated. Furthermore, Bragger and co-workers reported that alveolar bone loss was more advanced at a cle site compared with control, although the clinical attachment level was similar on both sites [25]. ese ndings suggested the presence of a longer connective tissue attachment in the cle regions. Reduced bone support might, however, cause several problems in the future in case of inadequate plaque control. us, professional evaluation and treatment, if required, is essential for maintaining the periodontal health of these patients.
According to Almeida and co-workers, the prevalence and severity of gingival recessions increased with age [26]. According to this study, the cle area did not present a higher prevalence and severity of gingival recession when compared with non-cle patients. In our results gingival recessions were absent. e main reason could be the thick structure of keratinized gingiva caused by scars a er surgery that protected gingival margins against root exposure. Areas with a narrow zone of keratinized gingiva may have a similar level of resistance to potential root exposure as gingiva with a wide zone in the case of the presence of the adequate thickness of the gingiva [27]. e study presented showed that even though the keratinized gingiva near the cle was narrow, there were no gingival recessions at adjacent teeth. However, one must remember that only in patients maintaining proper plaque control, the lack of a wide zone of gingiva would not result in clinical attachment loss and recessions [25,26,27]. Almeida and co-workers claimed that factors such as tooth position in the dental arch, the presence of fraena or scars, the absence of keratinized mucosa and traumatic tooth brushing might increase the prevalence of recession, however in their study the most a ected teeth were not adjacent to the cle s [28]. In another study the authors concluded that the prevalence of recession in teeth close to the cle was higher than the same teeth in patients without cle s, although the recessions were not severe [29]. Teeth at cle sites may present higher occurrence of gingival recession in the future, due to reduced bone support, as well as to the low quantity of mucosa [26,28,29].
Moreover, the reason for the lack of root exposure in our study could be related to the young age of the patients. e prevalence of gingival recession depends on  the level of oral hygiene, with a frequency between 12% and 19% in children, 15.5% to 54.5% in young adults, and 57.7% to 100% in older individuals. e high prevalence in older groups was related to the longer exposure of their teeth to etiologic factors of recessions [21]. ere is a potential risk that due to the presence of aetiological factors of recessions, children with cle s may develop gingival recession in the future [28].
In patients with a bilateral cle , the boundary structures of the oral vestibule are malformed [9,10]. Moreover, as a result of previous surgeries, such as cheiloplasty and bone gra ing, there might be even more limited space for a toothbrush, which combined with gingival folds favour food debris accumulation. An inadequately formed vestibule in cle patients causes additional stress from the malformed lips on the marginal gingiva on the labial teeth surfaces. is could lead to recession, periodontal disease and compromise the dentition status. A normal vestibule facilitates prosthodontic and orthodontic treatment [9]. In the study presented the vestibule was shallower near the teeth adjacent to the cle (second incisors and canines) in comparison to other teeth that were evaluated. It was di cult to assess the vestibular depth, because of mucosa folds, fraena, as well as teeth malposition. For that reason it could not be determined whether the presence of the cle alone decreased the vestibular depth, or whether it resulted from the presence of di erent factors. e presence of an orthodontic appliance, the sti ness of the upper lip due to scar formation, crowding and malformation of the teeth may hamper optimal oral hygiene [16,18]. So tissue folds and deformities of mucosa make tooth brushing di cult. ese areas constitute a habitat for food debris and bacteria accumulation and consequently increase the risk of periodontal infection and caries [20,22,23]. e results of the study presented indicated that oral hygiene was not optimal in patients ( g. 2). ese data were consistent with other studies that also recorded high scores for dental plaque in cle patients [20,22,23]. However, the di erences between cle and non-cle sites were small in the study assessing oral hygiene in unilateral cle patients [20]. It suggests that not only mucosa malformation but also young age and orthodontic appliances are the reasons for inadequate plaque control. Furthermore, according to Bragger and co-workers, due to inadequate oral hygiene, adult patients with cle s demonstrated early signs of periodontitis with furcation involvement in most of cases [30]. is is consistent with another study that showed that over a 14-year period cle sites in subjects with high plaque and gingival in ammation underwent more periodontal tissue destruction than control sites [21].
e study presented showed irregularities of the gingiva margin and so tissue at the teeth adjacent to the cle . ere were scars and mucosa folds in the vestibule, however pull-syndrome was not present et the marginal gingiva ( g. 1,2). ere were also atypical upper labial fraena and the biotype was di cult to assess. ese characteristics, which had been observed also by other authors, were present due to the cle itself, but also as a result of surgical treatment [9,11,18].

CONCLUSIONS
e results of the present study indicate that: 1. Malformations of hard and so tissue caused by the cle itself and previous surgical procedures have a negative in uence on periodontal parameters in the cle area. 2. Narrow gingiva and shallow vestibule at the cle site in the presence of dental plaque do not favour maintenance of a healthy periodontium. is corresponded with increased bleeding at some teeth adjacent to cle s. 3. It seems essential to include regular periodontal examination and prophylaxis into comprehensive treatment in cle patients. Further assessment of a large-sized group is necessary to establish the preventive protocol in multidisciplinary treatment. 2. Manuscripts should be sent to the editors' address in two copies of single-sided computer printouts, on A4 format paper with a margin of 4 cm on the left side and double space between the lines. Authors are asked to make the text available on electronic media and specify the word processor used, preferably be Word for Windows. Texts can be sent by e-mail. 5. The text of original research studies must have the following structure: introduction, aim, materials and methods, results, discussion, conclusions (which cannot be a summary of the paper). Abbreviations must be preceded by the full text when first used. In research studies in which investigations were carried out on human beings or animals, as well as in clinical studies, approval of the Bioethics Committee must be obtained and relevant information be included in the manuscript.

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